A new species of from Chocó, Colombia (Cycadales, )

1 2 1 MICHAEL CALONJE ,DENNIS STEVENSON ,CLAUDIA CALONJE , 3 2 YAN ARLEY RAMOS , AND ANDERS LINDSTROM

1 Author for correspondence: Montgomery Botanical Center, 11901 Old Cutler Road, Miami, FL 33156, U.S.A.; e-mail: [email protected] 2 The New York Botanical Garden, Bronx, NY 10458-5126, U.S.A. 3 Universidad Tecnológica del Chocó, Herbario CHOCO, Grupo de Investigación de la Flora Chocoana, Quibdó, Chocó, Colombia.

Abstract. Zamia pyrophylla, a new species from Chocó, Colombia, is described and illustrated. It is compared to Z. amazonum, Z. cunaria, and Z. ipetiensis.Itisdist- inguished by its bright orange and red emerging with leaflets that progress- ively turn green from the apex to the base as they mature, petioles with branched prickles and with ferruginous pubescence when immature, villous strobilar axes, and adaxial microsporangia. Key Words: , Chocó, Zamia.

Stevenson (2001) recognized 18 species of A research expedition led by the CHOCO in Colombia, 16 of these included in the herbarium of the Universidad Tecnológica del genus Zamia L., and two in the endemic genus ChocóinQuibdóincollaborationwithMont- Chigua D. W. Stev. Calderón-Sáenz and Steven- gomery Botanical Center (Miami, Florida) took son (2003) subsequently described Zamia oli- place in March of 2009 with the purpose of godonta, bringing the total of recognized species gaining a better understanding of this relatively in Colombia to 19. Six of these species (Z. unknown Zamia from the Chocó. Close exami- amplifolia W. Bull ex. Mast., Z. chigua Seem., nation of several hundred across five Z. disodon D.W. Stev. & Sabato, Z. obliqua A. different populations, including fertile plants Braun, and Z. roezlii Linden) occur in the Chocó with ovulate and pollen strobili, led us to the biogeographic region of Colombia. This region conclusion that this taxon represents a new stretches across the entire Pacific coast of species, formally described below. Colombia, including parts of the Departments of Chocó, Valle del Cauca, Cauca, Risaralda, Zamia pyrophylla Calonje, D.W. Stev. & A. Antioquia, Córdoba, and Nariño and is consid- Lindstr. sp. nov. Type: Colombia. Chocó: ered one of the most biologically diverse areas Mun. Quibdó, 60–100m, Calonje et al. COL09– on the planet. In addition to the species noted 014 (holotype: CHOCO; isotypes: COL, above, Stevenson (2001) also listed three Zamia CHOCO, CUVC, HUA). (Figs. 1, 2) collections made in Chocó (Bernal et al. 1090, COL; Juncosa 1721, JAUM, MO, NY; Santa et Zamia cunaria D. W. Stev. simulans, sed marginibus al. 1149, HUA.) under specimens examined for foliolii integerrimis et apice megasporophylli sterilis Zamia amazonum D. W. Stev., noting that the longate differt. material differed somewhat from the typical material and suggesting that further research Stem hypogeous, rarely branching, globose would be necessary to confirm whether this to cylindrical, to 10 cm or more in diameter. material represented a different species. Cataphylls chartaceous, triangular to narrowly

Brittonia, 62(1), 2010, pp. 80–85 ISSUED: 1 March 2010 © 2009, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A. 2010] CALONJE ET AL.: ZAMIA (ZAMIACEAE) 81

FIG.1. Vegetative features of Zamia pyrophylla. A. Seedling with eophyll and apogeotropic roots. B. Side view of characteristic . C. Frontal view of emergent leaf. D. Cataphylls. E. Median leaflet. F. Caudex of juvenile . All photographs taken of plants from type locality (Calonje et al. COL09–014). 82 BRITTONIA [VOL 62

FIG.2. Reproductive features of Zamia pyrophylla. A. Ovulate strobilus at near receptivity stage. B. Mature ovulate strobilus. C. Mature megasporophyll face, frontal view. D. Mature megasporophyll, abaxial view. E. Mature seed with sarcotesta. F. Sclerotesta of mature seed. G. Pollen strobilus at pollen shedding. H. Mature pollen strobilus cross-section, adaxial view. I. Mature pollen strobilus cross-section, abaxial view. J. Juvenile pollen strobili. K. Microsporophyll, adaxial view. L. Microsporophyll, abaxial view. All photographs taken of plants from type locality (Calonje et al. COL09–014). 2010] CALONJE ET AL.: ZAMIA (ZAMIACEAE) 83 triangular, to 8.5×3.0 cm, tan-tomentose with and white hairs, sterile apex 19–20 mm deep brown papyraceous wings. Ptyxis inflexed. with hexagonal to oblong-hexagonal distal face Leaves 1–2, 1.1–3.4 m long; petioles 12.5–13.2 x 15.5–16.2 mm, extruded to a 0.75–2.4 m long with abruptly swollen base to small, depressed terminal facet 2.5–3.4× 4 cm wide, densely covered with stout, some- 5.7–6.3 mm, megasporophyll face tomentose, times branching prickles to 5 mm long; rachis burnt amber in new strobili, rust colored when 0.3–1 m long, curved outward, with prickles in near receptivity, at maturity black with some lower half, petiole and rachis brown tomentose exposed areas glabrous green. Seeds ovoid, when emerging, gradually becoming glabrous. 10–15.6 mm×9.5–13.2 mm, sarcotesta red and Leaflets 8–16 pairs, chartaceous to coriaceous, fleshy, eventually becoming evenly papyra- median ones 2–5.8 cm apart, insertion on rachis ceous at maturity. 6–10 mm wide, lanceolate to oblanceolate and Distribution and habitat.—This species is straight to slightly falcate, alternate to subop- known only from the Atrato Valley in the posite, apex acute to acuminate, margins entire, Municipalities of Quibdó and Atrato, Chocó. basal leaflets 28–51×2.2–7.2 cm; median leaf- It occurs in tropical rainforest at elevations lets 24.5–55×4–7.1 cm; apical leaflets between 10–100 m. Because it has a sub- 19–34.5×2.1–6.6 cm wide, maroon at emer- terranean stem, it is able to survive initial gence, turning to orange or reddish tones, and forest clearing and can thrive and produce gradually turning green from the leaflet apex to strobili while growing in full sun in pastures the base as they mature. Eophylls with unarmed if left undisturbed. Plants were frequently petioles 19–25 cm long, rachis to 1 cm long, observed with emergent new leaves in typically carrying four leaflets 6.1–6.5× recently cleared fields, but were absent from 1.7–2.2 cm. Pollen strobili conical-cylindrical, older clearings, suggesting the plants may not erect or slightly spreading, 5–15 +, at pollen be able to survive repeated leaf excision from shedding 7.1–8.1×1.5–1.7 cm, strobilar axis pasture clearing. and proximal section of microsporophyll vil- The area near Quibdó is one of the wettest lous with mixed white and rust-brown hairs, on earth, with an average annual precipitation peduncles tomentose, emerging white to cream of 8558 mm (West, 1957). The drier season and maturing maroon to brown, 14–25× occurs from January through March with 0.8–1 cm, microsporophylls spirally arranged February being the driest month, and the in 8–10 orthostichies of 13–20 rainy season occurs April through December, each, obtrullate, 5.9–6.3×3.5–4.3 mm at pollen with August being the wettest month. The shedding, sterile apex encompassing 1/4 to 1/2 temperature averages 28°C and ranges from of total length of a microsporophyll, tomentose, 15°C to 41°C (Forero, 1982). tan to cream colored in proximal half, speckled Reproductive phenology.— Very little is maroon to brown in distal half, face hexagonal known about the reproductive phenology of to oblong hexagonal, 2.7–3×3.5–4 mm, this species. All herbarium specimens exam- extruded downward to a narrow horizontal ined prior to our March 2009 expedition were facet, abaxial side of microsporophyll with sterile with no mention of reproductive 15–20 microsporangia limited to the proximal structures in the label notes. During this half and along the margins, adaxial side with expedition, we were fortunate to observe both 12–15 microsporangia limited to the distal half. seed and pollen strobili at all stages of Ovulate strobili cylindrical, typically solitary maturity. Further research is required in order but up to 3 per crown, erect at maturity, to determine whether there is any periodicity 8–15.5×4–4.5cm,sterileapex0.5–4cmand in the timing of the reproductive events of acute to acuminate, strobilus axis villous with this species. mixed rust-brown and white hairs, peduncles Ecology.—Larvae of a species of Eumaeus 15–50×1.2–2.7 cm, emerging white to cream Hübner were observed feeding on emergent tomentose, progressing maroon to brown Zamia leaves and live butterflies were tomentose, at maturity appearing green due to observed laying eggs on new leaves and loss of tomentum, megasporophylls in 7–10 emergent pollen strobili. Pollen strobili at orthostichies of 5–11 sporophylls each, stalk pollen release stage were observed harboring 8–10 mm long, villous with mixed rust-brown numerous clavicorn beetles of the genus 84 BRITTONIA [VOL 62

Pharaxonotha Reitt., known pollinators of two species have margins that are distinctly other Zamia species (Vovides, 1991; Tang, toothed on the upper half. The petiole and 1987; Stevenson et al., 1998). rachis of Z. pyrophylla is densely covered with Etymology.—The specific epithet refers to a ferruginous pubescence on young leaves and the glowing orange and red emergent leaves, have branched prickles, whereas those of Z. which progressively turn green from the apex cunaria and Z. ipetiensis are lightly covered to the base, giving them a fiery appearance. with a white pubescence and have unbranched Conservation status.—This species has prickles. The microsporophylls of Z. cunaria been collected only in an area covering and Z. ipetiensis are a uniform tan or cream approximately 25 km2 in the Municipalities color at pollen shed, whereas those of Z. of Quibdó and Atrato. It is quite common at pyrophylla are tan or cream colored on the some localities, and evidence of seedling proximal half of the sterile apex turning to establishment was observed in forested maroon or brown on the distal half. The ovulate areas. However, it is directly threatened by strobili of Z. pyrophylla typically has an acute agricultural expansion and other habitat or acuminate apex, and megasporophyll faces transformations. Based on its poorly known that are strongly extruded outward, whereas the but currently restricted extent of occurrence strobili of Z. cunaria and Z. ipetiensis typically and area of occupancy, this species should be have obtuse apices and megasporophyll faces listed as Critically Endangered (CR) based on that are more or less flat or only slightly IUCN Red List criteria B1b+2b (IUCN, extruded. Finally, Z. pyrophylla has leaves 2001). Additional field work is necessary to attaining a maximum length of 3.4 m long, determine the geographic range and compared to those of Z. cunaria which reach abundance for this species. 2.5 m in length, and those of Z. ipetiensis, which attain a maximum of 1.7 m in length Additional specimens examined. COLOMBIA. (Alberto Taylor, pers. comm.). Chocó: Bernal et al. 1090 (CHOCO, COL, FTG, NY); Early collections of this species were dis- – — Municipio del Atrato, 80 90m, Calonje et al. COL09 cussed under Zamia amazonum by Stevenson 001 (CHOCO, COL); Municipio de Quibdó, 80–100m, Calonje et al. COL09—021 (CHOCO); Kress & Eche- (2001), who noted that additional research verry 89–2571 (CHOCO); Santa et al. 1149 (HUA). would be necessary to understand whether the taxon collected in Chocó belonged to a different Collections made 100 km NW of Quibdó species. Zamia amazonum and Z. pyrophylla (Juncosa 1721, CHOCO, JAUM, MO, NY) both have hypogeous stems, carry few leaves at differ from the type material in having leaflets a time, leaflets with entire margins, densely with toothed margins at the distal end. In tomentose petioles and rachises on young addition, the specimen label mentions that leaves, and stout, occasional branched prickles leaves of adult plants typically carry 4 leaflet on the petiole. However, Zamia amazonum can pairs, whereas Z. pyrophylla typically carries be differentiated from Z. pyrophylla because it 8–16. Further fieldworkisrequiredto carries 2–6 leaves with up to 30 leaflet pairs, has determine if these collections represent this glabrous strobilar rachises, and no micropor- species or a different one. angia on the adaxial surface of the micro- Zamia pyrophylla most closely resembles sporophylls, whereas Z. pyrophylla carries 1–2 Zamia cunaria D.W. Stev. and Zamia ipe- leaves with up to 18 leaflet pairs, has villous tiensis D.W. Stev. from adjacent Panama. All strobilar axes, and microsporangia present on three species typically carry one leaf at a the adaxial surface of the microsporophylls. time, have subterranean stems, small seeds Villous strobilar axes are a rare feature in with a paper-thin sarcotesta, microsporangia Zamia, only observed by the authors in Z. present on both the abaxial and adaxial pyrophylla, Z. cunaria,andZ. ipetiensis.The surfaces of microsporophylls, villous axes in presence of microsporangia on the adaxial both the pollen and ovulate strobili, and surface of the microsporophylls is also uncom- seedlings that produce long apogeotropic mon, occurring in only eight of 68 recognized roots. Zamia pyrophylla is easily differenti- species of Zamia, namely Z. cunaria, Z. ated from the Panamanian species as it has encephalartoides D.W. Stev., Z. fairchildiana leaflets with entire margins whereas the other L.D. Gómez, Z. pyrophylla, Z. hymenophyllidia 2010] CALONJE ET AL.: ZAMIA (ZAMIACEAE) 85

D.W. Stev., Z. melanorrachis D.W. Stev., Z. herbarium specimens. The following UTCH obliqua A. Braun, and Z. pseudomonticola alumni accompanied us on the expedition and L.D. Gómez. provided us with much needed assistance: The bright orange and red-emergent leaflets Yessid Rayo Pino, Reimer Rengífo Ibargüen, that turn green from the apex to the base as Yuber Palacios Torres, Jorge Enríque García they mature are a unique feature of Z. Arias, and Elmer Rentería Maturana. This pyrophylla. In contrast, plants of Zamia research was supported in part by NSF Grants amazonum have brown-emergent leaflets that BSR-8607049 and EF-0629817 to DWS. turn green from the base to the apex, whereas Zamia cunaria and Z. ipetiensis typically fl have green emergent lea ets and occasionally Literature Cited brown-emergent leaflets that turn green from Calderón-Sáenz, E. & D. W. Stevenson. 2003. Una the apex to the base. Most species of Zamia nueva especie del género Zamia L. (Zamiaceae), de with brown-emergent leaves have leaflets that los Andes de Colombia y clave actualizada para las either gradually and evenly turn green or do especies del género en Colombia. Revista Acad. so from the base to the apex. Colomb. Ci. Exact. 27: 485–490. Forero, E. 1982. La flora y la vegetación del Chocó y For the time being, the relationship of sus relaciones fitogeográficas. Colombia Geográfica, Zamia pyrophylla to other species of Zamia Revista Instituto Geográfico Agustín Codazzi 10: 77– is enigmatic. However, research into a com- 90. bined analysis of molecular and morpholog- IUCN. 2001. IUCN Categories & Criteria, ver. 3.1. ical data that is now in progress should IUCN Species Survival Commission, Gland, Switzer- land. Website: < http://www.redlist.org/info/ elucidate the species relationships within categories_ criteria2001.html >. Accessed 16 October Zamia and in turn lead to a better under- 2008. standing of their historical biogeography. Stevenson, D. W. 2001. Cycadales. Flora de Colombia 21: 1–92. ———, K. Norstog & P. Fawcett. 1998. Pollination Acknowledgments biology of cycads. In S. Owens & P. Rudall (eds.), Reproductive Biology: In systematics, conservation, The expedition resulting in this description and economic botany. Royal Botanic Gardens, was a collaborative venture between the Kew. Universidad Tecnológica del Chocó (UTCH) Tang, W. 1987. Insect pollination in the cycad Zamia pumila (Zamiaceae). American Journal of Botany 74: and Montgomery Botanical Center (MBC) as 90–99. part of the “Proyecto Estudio Integral de la Vovides, A. P. 1991. Insect symbionts of some Mexican Flora del Chocó” with generous support from cycads in their natural habitat. Biotropica 23(1): 102– Francois and Angela Dolmetsch and the Zane 104. West, R. C. 1957. The Pacific lowlands of Colombia: a B. Carothers Memorial Fund. The CHOCO Negroid area of the American tropics. Louisiana State herbarium at UTCH provided workspace and Univ. Studies, Soc. Sci. Ser. No. 8. Louisiana State herbarium infrastructure for preservation of University Press, Baton Rouge. 278 pp